IAJPS 2017, 4 (11), 4326-4332 Raziani vahid et al ISSN 2349-7750

CODEN [USA]: IAJPBB ISSN: 2349-7750

INDO AMERICAN JOURNAL OF

PHARMACEUTICAL SCIENCES
http://doi.org/10.5281/zenodo.1064022

Available online at: http://www.iajps.com Research Article

PERIODONTAL CLINICAL CHARACTERISTICS IN PATIENTS

WITH IRON DEFICIENCY ANEMIA
Torkzaban, parviz1, Janet Moradi Haghgoo2, Mohamad Abbasi3, Raziani, vahid4*
1
Associate Professor and Member of Hamadan Dental Research Center, Dept. of Priodontology , Faculty
of Dentistry,Hamadan University of Medical Sciences, Fahmideh Blv, Hamadan, Iran. Tel: +98 811
8381081 Email: p.torkzaban@umsha.ac.ir
2
Department of Periodontics, School of Dentistry, Hamedan University of Medical Sciences, Hamadan,
Iran
3
School of Medicin University of Medical Sciences, Fahmideh Blv, Hamadan, Iran.
Khalil Rostai Dentist
*4 Pstgraduate student of periodontics, Dept. of Priodontology, Faculty of Dentistry,Hamadan University
of Medical Sciences, Fahmideh Blv, Hamadan, Iran.
Abstract:
The main aim of this study was to evaluate the periodontal clinical characteristics in patients with iron deficiency anemia.
In a cross-sectional study, 280 consecutive patients suffered iron deficiency anemia and referred to Sina hospital in Hamadan,
Iran between April and October 2012 were included into the study. Iron-deficiency anemia was defined as a hemoglobin
concentration 12.5 g per deciliter for men (normal range, 13.5 to 17.5 [8.4 to 10.9]) and 10.6 g per deciliter for women
(normal range, 11.6 to 15.8 [7.2 to 9.8]), accompanied by at least one of the following laboratory values consistent with iron
deficiency: a serum iron concentration 45 g per deciliter (normal range, 50 to 150 [9.0 to 27.0]) with a transferrin saturation
no higher than 10 percent (normal range, 16 to 60 percent), a serum ferritin concentration 20 g per liter for men (normal
range, 20 to 450) and 10 g per liter for women (normal range, 10 to 250), or the absence of iron stores in bone marrow-
biopsy specimens [10]. None of the participants were smoker.
Several clinical and experimental studies have documented the mechanisms which predisposing oral alterations in patients with
iron deficiency anemia [13]. Most of these mechanisms involve cell-mediated immune effectors pathways and cytokines. In fact,
various cytokines, acute-phase proteins and radicals with regulatory effects on iron-homeostasis may be altered following
periodontal inflammatory or infectious states resulting in anemia Several clinical and experimental studies have documented the
mechanisms which predisposing oral alterations in patients with iron deficiency anemia. On the other hand, the release of these
cytokines by periodontal tissues in response to bacterial infection can be the main fundament of periodontal disease-induced
anemia.
Key words: Gingiva, mouth mirrors, plaque control record (PCR) and buccal.
Corresponding author:
Raziani vahid, QR code
Postgraduate Student of Periodontics,
Dept. of Priodontology, Faculty of Dentistry,
Hamadan University of Medical Sciences,
Fahmideh Blv, Hamadan, Iran.
Tel:+989163234112
Email:vahidraziani@gmail.com
Please cite this article in press as Raziani vahid et al., Periodontal Clinical Characteristics in Patients with Iron
Deficiency Anemia , Indo Am. J. P. Sci, 2017; 4(11).

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 IAJPS 2017, 4 (11), 4326-4332
INTRODUCTION:
Periodontal diseases as multifactorial phenomena are
potentially affected by a wide variety of factors
including baseline characteristics, social and
behavioral indicators, and even genetic predisposing
factors [1]. These disease are also associated with
several systemic disorders and thus systemic medical
evaluation of the patients with periodontal disease is
usually advisable. This approach not only makes
access to dental health, but also prevents further
dental losses [2,3]. Various former and recent studies
evidenced relationship between iron deficiency
anemia and periodontal disease [4,5]. In susceptible
patients, it has been demonstrated that subgingival
microbial colonization can induce infectious
condition of the supporting tissues of the teeth that
result in immune inflammatory response to bacteria
and their products [6]. Therefore, the inflammatory
biomarkers as cytokines are produced and secreted
during periodontal inflammation that may depress
erythropoietin production leading to the development
of anemia. On the other hand, a lower number of
erythrocytes and hemoglobin levels in those with
periodontal disease are predictable compared to
healthy controls [7]. Meanwhile, it is now
hypothesized that the periodontal therapies may
effectively improve the anemic status of these
patients [8,9]. However, a few studies assessed
clinical and periodontal evidences in anemic patients.
The present study evaluated periodontal clinical
characteristics in patients with iron deficiency anemia
to more reveal the periodontal changes leading to the
development and worsening anemia.
METHODS:
In a cross-sectional study, 280 consecutive patients
suffered iron deficiency anemia and referred to Sina
hospital in Hamadan, Iran between April and October
2012 were included into the study. Iron-deficiency
anemia was defined as a hemoglobin concentration
12.5 g per deciliter for men (normal range, 13.5 to
17.5 [8.4 to 10.9]) and 10.6 g per deciliter for
women (normal range, 11.6 to 15.8 [7.2 to 9.8]),
accompanied by at least one of the following
laboratory values consistent with iron deficiency: a
serum iron concentration 45 g per deciliter
(normal range, 50 to 150 [9.0 to 27.0]) with a
transferrin saturation no higher than 10 percent
(normal range, 16 to 60 percent), a serum ferritin
concentration 20 g per liter for men (normal
range, 20 to 450) and 10 g per liter for women
(normal range, 10 to 250), or the absence of iron
stores in bone marrow-biopsy specimens [10]. None
of the participants were smoker. Those with any
systemic disorders that might affect the periodontal
tissues were excluded. The study was reviewed and
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Raziani vahid et al ISSN 2349-7750
approved by the ethical committee of the faculty of
dentistry, Hamadan University of Medical Sciences.
Patients were advised of their role and asked to
provide written informed consent. Baseline
information including demographics, medical history,
and duration of anemia was collected by interviewing
and recorded in study questionnaire. Fool mouth
examinations were conducted for all patients. The
main study periodontal parameters included: plaque
control record, bleeding on probing, probing depths,
clinical attachment level, gingival color, gingival
consistency, gingival contour, gingival size, as well
as gingival texture. Gingival state was examined
using an especial Williams periodontal probe
disposable mouth mirrors and all gingival sites were
evaluated. For assessment of plaque control record
(PCR), following consumption of disclosing tablet
and appearance of plaques, four dental surfaces of
buccal, lingual, mesial, and distal were evaluated and
PCR was calculated by the following formula:
PCR = [number of colored surfaces / (number of
all teeth 4)] 100%
Probing technique was also applied to assess correct
depth of pocket. Using the William periodontal probe
and mouth mirrors, the medial, mesial, and distal
sites of the buccal and lingual surfaces were
examined and depth of dental plaque was recorded.
Gingival bleeding was also assessed using the
gingival bleeding index (GBI) using the following
formula:
GBI = [number of bleeding sites/ (number of all
teeth 4)] 100%
Moreover, for assessing clinical attachment level, the
selected reference was CEJ that the distance between
pocket depth and CEJ was determined in six medial,
mesial, and distal sites of buccal and lingual surfaces
using the William periodontal probe. As noted, all
measurement was performed using the same William
probe graded from 1 to 10 mm.
RESULTS:
With regard to demographics characteristics, the
average age of the participants was 30.4 15.4 years
that most of them (77.1% were female). More than
half of the patients experienced iron deficiency
anemia more than one year, while only 34.2% of
subjects suffered from anemia less than one year
(Table 1). The majority of patients had oral habits
such as lip biting, cheek biting, and finger nail biting.
Method of brushing in 92% of the participants was
reported as rolling and only 4% of them regularly
used the bass method.
As shown in Table 2 and with respect to gingival
color, the most frequent detected color in the studied
sites including right posterior, left posterior, and
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anterior sites was red (ranged between 57.1% and
66.4%), followed by pale pink color that was
detected in 32.8% to 42.9% of the cases. Regarding
gingival consistency, the most common form of
consistency in left and right posterior regions was
spongy form and in anterior region was firm form. In
this regard, fibrotic form was rarely observed.
Scalloped contour was commonly seen in anterior
region, while non-scalloped contour was more
detected in posterior regions. In addition, stippled
texture was reported in 61.0% in anterior region,
whereas only 26.9% in right posterior and 27.3% in
left posterior regions. Normal gingival size was
detected in 66.3% in anterior region, while about
two-third of left and right posterior regions had
recessed gingival and gingival enlargement was not
found in any of the studied gingival regions. Also,
with regard to atrophy of gingival papillae, this
phenomenon was found 8.2% in anterior region and
56.3% in posterior regions.
Table 1: Baseline characteristics of study population (N = 280)
Gender
Men
Women
Age
Oral habits
Method of brushing
Rolling method
Bass method
Other methods
Duration of anemia
Less than 1 year
1 to 3 years
3 to 5 years
More than 5 years
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Raziani vahid et al ISSN 2349-7750
Regarding common tongue clinical features, the most
prevalent feature was burning tongue (30.0%),
followed by lip fissure without burning (Figure 1).
The mean plaque control record in anemic subjects
was 62.5 19.1 (ranged 41 to 179) and the mean
bleeding probe index was 50.8 11.6 (ranged 26 to
100).
In maxilla, the average ranges of CAL index in
superior buccal was between 0.36 mm and 2.87 mm,
and in superior palatal was between 0.33 mm and
2.72 mm (Table 3). Also, the mean maxillary PD
index in superior buccal and superior palatal was
ranged 0.38 to 2.68 mm and 0.38 to 2.44 mm,
respectively. The same examination in mandible
showed that the mean mandibular CAL index ranged
0.99 to 2.88 for superior buccal and 0.97 to 2.87 for
superior palatal site. Also, mandibular BD index
ranged between 1.47 and 2.73 mm for superior
buccal and between 0.87 and 2.68 mm for superior
palatal region.
65 (22.9)
214 (77.1)
30.4 /15.47
214 (76.5)
258 (92.1)
11 (3.8)
11 (3.8)
96 (34.2)
152 (54.4)
29 (10.3)
3 (1.1)
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Table 2: Baseline gingival pattern of study population (N = 280)

Gingival pattern Right posterior Anterior Left posterior

(up and down) (up and down) (up and down)
Gingival color
Pale pink 88 (32.8) 115 (42.9) 88 (32.8)
Dark pink 2 (0.8) 0 (0.0) 2 (0.8)
Red 178 (66.4) 153 (57.1) 178 (66.4)
Bluish 0 (0.0) 0 (0.0) 0 (0.0)
Gingival consistency
Firm 120 (44.9) 196 (73.4) 122 (45.7)
Spongy 146 (54.7) 71 (26.6) 145 (54.3)
Fibrotic 1 (0.4) 0 (0.0) 0 (0.0)
Gingival contour
Scalloped 81 (30.3) 197 (73.8) 83 (31.1)
Non-scalloped 183 (68.5) 70 (26.2) 181 (67.7)
Knife edge 0 (0.0) 0 (0.0) 0 (0.0)
Round edge 3 (1.2) 0 (0.0) 3 (1.2)
Gingival texture
Stippled 72 (26.9) 163 (61.0) 73 (27.3)
Non-stippled 195 (73.1) 104 (39.0) 194 (72.7)
Gingival size
Normal 93 (34.9) 177 (66.3) 96 (36.0)
Recessed 174 (65.1) 90 (33.7) 171 (64.0)
Enlarged 0 (0.0) 0 (0.0) 0 (0.0)
Atrophy of gingival papillae 143 (56.3) 21 (8.2) 143 (56.3)

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Table 3: CAL and PD indices in study population (N = 280)

Number of tooth CAL PD CAL PD

(superior buccal) (superior buccal) (superior palatal) (superior palatal)
Mean/SD Mean/SD Mean/SD
Mean/SD
Maxilla
28 0.36/1.80 0.38/0.89 0.33/1.05 0.38/0.92
27 2.43/1.81 1.88/1.49 2.35/1.85 1.88/1.49
26 2.63/1.06 1.87/1.46 2.03/1.75 1.78/1.48
25 2.78/0.94 2.61/0.73 2.67/0.85 2.36/0.67
24 2.74/1.02 2.58/0.73 2.57/0.86 2.30/0.73
23 2.44/0.97 2.53/0.54 2.72/0.79 2.38/0.56
22 2.63/1.07 2.47/0.89 2.45/0.99 2.30/0.84
21 2.75/1.17 2.56/1.01 2.44/1.09 2.33/0.99
11 2.87/1.05 2.68/0.87 2.56/1.01 2.44/0.89
12 2.62/1.06 2.50/0.84 2.45/1.00 2.23/0.85
13 2.55/0.99 2.46/0.55 2.69/0.79 2.34/0.55
14 2.68/1.06 2.45/0.78 2.53/0.97 2.33/0.77
15 2.80/0.96 2.59/0.69 2.70/0.88 2.39/0.67
16 1.95/1.73 1.73/1.52 1.89/1.74 1.64/1.49
17 2.70/1.78 2.11/1.45 2.53/1.77 1.99/1.40
18 0.38/1.14 0.33/0.96 0.38/1.10 0.26/0.85
Mandible
38 0.99/1.67 1.47/0.78 0.97/1.68 0.87/1.49
37 2.43/1.82 2.02/1.55 2.42/1.77 2.02/1.56
36 1.13/1.57 1.08/1.47 1.12/1.53 1.11/1.50
35 2.87/0.92 2.68/0.63 2.79/0.98 2.66/0.72
34 2.57/1.11 2.44/0.93 2.54/1.13 2.44/0.96
33 2.41/1.01 2.59/0.55 2.87/0.82 2.68/0.59
32 2.87/0.92 2.70/0.63 2.81/0.87 2.62/0.67
31 2.88/1.00 2.72/0.74 2.80/0.97 2.55/0.79
41 2.86/0.97 2.73/0.73 2.84/0.96 2.60/0.71
42 2.88/0.89 2.70/0.65 2.84/0.88 2.64/0.68
43 2.44/1.09 2.54/0.55 2.90/0.81 2.68/0.59
44 2.73/1.12 2.48/0.85 2.68/1.00 2.53/0.87
45 2.87/1.01 2.59/0.77 2.81/0.98 2.61/0.83
46 1.55/1.78 1.38/1.54 1.55/1.67 1.43/1.59
47 2.48/1.81 2.08/1.51 2.50/2.43 2.10/1.57
48 0.91/1.66 0.74/0.36 0.87/1.60 0.79/1.43

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Figure 1: Patterns of Tongue in anemic patients with periodontal disorders (SSRBT: Smooth, shiny, and red
with burning tongue; SSRBTLF: Smooth, shiny, and red without burning tongue and lip fissure; SSRLF:
Smooth, shiny, and red with lip fissure; SSRRLC: Smooth, shiny, and red with red lip corner; SSRBTO:
Smooth, shiny, and red with burning tongue and Odynophagia; SSRWBTO: Smooth, shiny, and red without
burning tongue and Odynophagia; SSRP: Smooth, shiny, and red with papillae; SSRPAU: Smooth, shiny,
and red with papillae with aphthous ulcers)

DISCUSSION: mediated immune effectors pathways and cytokines.

New studies have suggested that periodontal disease
lead to reduction in red blood cells production and
serum hemoglobin levels leading to iron deficiency
anemia. Some studies showed that more than a third
of people suffering from severe periodontitis had
hemoglobin levels below normal concentrations that
women are at more increased risk of anemia [6].
Thomas et al. found that periodontitis patients have
lower hematocrit, lower numbers of erythrocytes,
lower hemoglobin levels and higher erythrocyte
sedimentation rates when compared to healthy
controls [11]. Rai and Kharb revealed increased in
hemoglobin and RBC levels in patients with severe
periodontitis after scaling and root planning [12].
Also, Agarwal et al. demonstrated a significant
improvement in hemoglobin value and erythrocyte
count after periodontal treatment [8]. Interestingly,
the manifestation of iron deficiency anemia can
primarily recognized by dental examination before its
more clinical pronounced systemic manifestations
and this issue is very important in terms of clinical
evaluation of anemia.
Several clinical and experimental studies have
documented the mechanisms which predisposing oral
alterations in patients with iron deficiency anemia
[13]. Most of these mechanisms involve cell-
In fact, various cytokines, acute-phase proteins and
radicals with regulatory effects on iron-homeostasis
may be altered following periodontal inflammatory
or infectious states resulting in anemia [14]. On the
other hand, the release of these cytokines by
periodontal tissues in response to bacterial infection
can be the main fundament of periodontal disease-
induced anemia.
For assessing periodontal characteristics of anemic
patients, the current study was conducted that
revealed some important gingival changes in these
patients population. First, we observed more
incidence of anemia in affected women than men that
was also previously documented [6]. The mean age
of affected patients was 30 years as well as mean
duration of anemia was less than 3 years explaining
the early occurrence of anemia following periodontal
disorders. Regarding tongue features, burning
sensation in the tongue and lip fissure were the most
prevalent symptoms in anemic patients with
periodontal disorders. These manifestations have
been commonly showed in iron deficiency anemic
patients [15,16]. We also found that the method of
brushing in most of the patients was rolling. It seems
that improper brushing pattern result in inappropriate
changes in the gums and teeth grinding that

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 IAJPS 2017, 4 (11), 4326-4332
predispose to oral and dental inflammation and
infection. With respect to gingival characteristics,
prominent gingival color was red pink, prominent
consistency was spongy, prominent gingival contour
was non-scalloped, prominent texture was non-
stippling, and prominent gingival size was recessed.
These findings can certainly help clinicians to early
predict dental and gingival evidences of iron
deficiency anemia in those with periodontal
disorders. Meanwhile, according to the measurement
of GBI and CPR indices, most of the patients
suffered from bleeding within probing that might be
an introduction for more progression and severity of
anemia in these patients.
REFERENCES:
1.Nunn M. Understanding the etiology of
periodontitis: an overview of periodontal risk factors.
Periodontol 2000 2003;32:11-23.
2.Page RC. The pathology of periodontal diseases
may affect systemic diseases: inversion of a
paradigm. Ann Periodontol 1998;3:108-120.
3.Hatipoglu H, Hatipoglu MG, Cagirankaya LB,
Caglayan F. Severe periodontal destruction in a
patient with advanced anemia: A case report. Eur J
Dent. 2012 Jan;6(1):95-100.
4.Evaluation of systemic markers related to anemia
of chronic disease in the peripheral blood of smokers
and non-smokers with chronic periodontitis. Eur J
Dent 2008;2:102-109.
5.Hutter JW, van der Velden U, Varoufaki A, Huffels
RA, Hoek FJ, Loos BG. Lower numbers of
erythrocytes and lower levels of hemoglobin in
periodontitis patients compared to control subjects. J
Clin Periodontol. 2001 Oct;28(10):930-6.
6.Pradeep AR, Anuj S. Anemia of chronic disease
and chronic periodontitis: does periodontal therapy
www.iajps.com
Raziani vahid et al ISSN 2349-7750
have an effect on anemic status? J Periodontol. 2011
Mar;82(3):388-94. Epub 2010 Sep 15.
7.Gokhale SR, Sumanth S, Padhye AM. Evaluation
of blood parameters in patients with chronic
periodontitis for signs of anemia. J Periodontol. 2010
Aug;81(8):1202-6.
8.Agarwal N, Kumar VS, Gujjari SA. Effect of
periodontal therapy on hemoglobin and erythrocyte
levels in chronic generalized periodontitis patients:
An interventional study. J Indian Soc Periodontol
2009;13:6-11.
9.Lu S-Yu, Eng HL. Dramatic recovery from severe
anemia by resolution of severe periodontitis. J Dent
Sci 2010;5:4146.
10.Rockey DC, Cello JP. Evaluation of the
Gastrointestinal Tract in Patients with Iron-
Deficiency Anemia. New Eng J Med 1993;329:1691-
5.
11.Thomas B, Ramesh A, Ritesh K. Relationship
between periodontitis and erythrocyte count. JISP
2006;10:288-91.
12.Rai B, Kharb S. Effect of Scaling and Root
Planning in Periodontitis on Peripheral Blood. IJDS
2008; 6(1).
13.Weiss G. Modification of iron regulation by the
inflammatory response. Best Pract Res Clin
Haematol 2005;18:183-201.
14.Barry W.E. Iron Deficiency Anemia and Anemia
of Chronic Disease In: KayeD. & Rose LF, eds.
Internal Medicine for Dentistry, 2. Ed, St Louis:
Mosby Company, 1990:285-287.
15.Cavalcanti DR, Birman EG, Migliari DA, da
Silveira FR. Burning mouth syndrome: clinical
profile of Brazilian patients and oral carriage of
Candida species. Braz Dent J. 2007;18(4):341-5.
16.Jung H. Differential diagnosis of the "burning
tongue. Fortschr Med. 1972 Oct 19;90(29):1043-6.
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